Mammalian Biology

, Volume 93, Issue 1, pp 82–92 | Cite as

Differentiation underground: Range-wide multilocus genetic structure of the silvery mole-rat does not support current taxonomy based on mitochondrial sequences

  • Josef BryjaEmail author
  • Hana Konvičková
  • Anna Bryjová
  • Ondřej Mikula
  • Rhodes Makundi
  • Wilbert N. Chitaukali
  • Radim šumbera
Original investigation


The silvery mole-rat (Heliophobius argenteocinereus) is a solitary subterranean rodent with its distribution centred mainly in miombo woodlands of eastern Africa. This part of the continent was significantly influenced by the formation of the East African Rift System (EARS) during the last 25 Mya and by pronounced climatic changes in the Plio-Pleistocene that have caused genetic differentiation leading even to speciation events in many organisms. Recently, based on analysis of mitochondrial (mt) DNA sequences, it was suggested that H. argenteocinereus is a complex of six to eight species that diverged from the early to middle Miocene. In the present study, we significantly extended the sampling, re-analysed mtDNA datasets and analysed nuclear markers with the aim to assess the evolutionary history of Heliophobius. If we do not consider the old museum samples from south-eastern Democratic Republic of Congo (very divergent short mtDNA sequences obtained from ancient DNA, requiring further study from fresh material), the genus Heliophobius is composed of three major mtDNA lineages with parapatric distribution. The Rukwa Rift (+Mbeya triple junction) at the Zambia-Tanzania border, Lake Malawi, and the Eastern Arc Mountains form the biogeographical divides among these clades. The relatively shallow differences among the mitochondrial clades, divergence dating based on the use of the fossilised birth-death ratio model and a multi-locus dataset, and a very similar pattern of genetic structure to other rodents inhabiting the same area and habitat, suggest that the evolutionary history of the extant silvery mole-rat was predominantly influenced by the climatic fluctuations in the Plio-Pleistocene. Awaiting further studies employing genomiC., ecological, morphological or behavioural data, we advocate for using the single name H. argenteocinereus for all evolutionary lineages within this taxon, because ( 1 ) comparison of the genetic structure observed in mtDNA and nuclear markers suggest hybridization between at least some mtDNA lineages in the contact zones; and (2) new samples close to the type localities suggest incorrect use of previous names.


Bathyergidae Divergence dating Miombo Plio-Pleistocene climatic fluctuations Species delimitation 


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.


  1. Barbière, F., Marivaux, L., 2015. Phytogeny and evolutionary history of hystricognathous rodents from the Old World during the tertiary: new insights into the emergence of modern “phiomorph” families. In: Cox, P., Hautier, L. (Eds.), Evolution of the Rodents: Advances in Phylogenetics, Functional Morphology and Development, vol. 5. Cambridge University Press, pp. 87–138.CrossRefGoogle Scholar
  2. Bouckaert, R.R., 2010. DensiTree: making sense of sets of phylogenetic trees. Bioinformatics 26, 1372–1373.CrossRefGoogle Scholar
  3. Bouckaert, R., Heled, J., Khmery, D., Vaughan, T., Wu, C., Xie, D., Suchard, M.A., Rambaut, A., Drummond, A.J., 2014. BEAST 2: a software platform for Bayesian evolutionary analysis. PLoS Comput. Biol. 10, e1003537.CrossRefPubMedPubMedCentralGoogle Scholar
  4. Brugal, J.P., Denys, C., 1989. Vertébrés du site acheuléen d’Isenya (Kenya, District de Kajiado) - implications paléoécologiques et aléobiogéographiques. Comptes. Rendus. Biologies. (Paris, s. II) 308, 1503–1508.Google Scholar
  5. Bryja, J., Mikula, O., Sumbera, R., Meheretu, Y., Aghová, T., Lavrenchenko, L.A., Mazoch, V., Oguge, N., Mbau, J.S., Welegerima, K., Amundala, N., Colyn, M., Leirs, H., Verheyen, E., 2014. Pan-African phylogeny of Mus (subgenus Nannomys) reveals one of the most successful mammal radiations in Africa. BMC Evol. Biol. 14, 256.CrossRefPubMedPubMedCentralGoogle Scholar
  6. Colangelo, P., Verheyen, E., Leirs, H., Tatard, C., Denys, C., Dobigny, G., Duplantier, J.M., Brouat, C., Granjon, L., Lecompte, E., 2013. A mitochondrial phylogeographic scenario for the most widespread African rodent, Mastomys natalensis. Biol. J. Linn. Soc. Lond. 108, 901–916.CrossRefGoogle Scholar
  7. Cracraft, J., 1997. Species concepts in systematics and conservation biology—an ornithological viewpoint. In: Claridge, M.F., Dawah, H.A., Wilson, M.R. (Eds.), Species: The Units of Biodiversity. Chapman & Hall, London, United Kingdom, pp. 325–340.Google Scholar
  8. deMenocal, P.B., 2004. African climate change and faunal evolution during the Pliocene-Pleistocene. Earth Planet. Sci. Lett. 220, 3–24.CrossRefGoogle Scholar
  9. Drummond, A.J., Ho, S.Y.W., Phillips, M.J., Rambaut, A., 2006. Relaxed phylogenetics and dating with confidence. PLoS Biol. 4, e88.CrossRefPubMedPubMedCentralGoogle Scholar
  10. Dubach, J., Patterson, B.D., Briggs, M.B., Venzke, K., Flamand, J., Stander, P., Scheepers, L., Kays, R.W., 2005. Molecular genetic variation across the southern and eastern geographic ranges of the African lion, Panthera ieo. Conserv. Genet. 6, 15–24.CrossRefGoogle Scholar
  11. Evanno, G., Regnaut, S., Goudet, J., 2005. Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol. Ecol. 14, 2611–2620.CrossRefGoogle Scholar
  12. Faulkes, C.G., Bennett, N.C., Bruford, M.W., O’Brien, H.P., Aguilar, G.H., Jarvis, J.U.M., 1997. Ecological constraints drive social evolution in the African mole-rats. Proc. R. Soc. Lond. B 264, 1619–1627.CrossRefGoogle Scholar
  13. Faulkes, C.G., Verheyen, E., Verheyen, W., Jarvis, J.U.M., Bennett, N.C., 2004. Phylogeographical patterns of genetic divergence and speciation in African mole-rats (Family: Bathyergidae). Mol. Ecol. 13, 613–629.CrossRefGoogle Scholar
  14. Faulkes, C.G., Bennett, N.C., Cotterill, F.P.D., Stanley, W., Mgode, G.F., Verheyen, E., 2011. Phylogeography and cryptic diversity of the solitary-dwelling silvery mole-rat, genus Heliophobius (family: Bathyergidae). J. Zool. 285, 324–338.CrossRefGoogle Scholar
  15. Gavryushkina, A., Welch, D., Stadler, T., Drummond, A.J., 2014. Bayesian inference of sampled ancestor trees for epidemiology and fossil calibration. PLoS Comput. Biol. 10, e1003919.CrossRefPubMedPubMedCentralGoogle Scholar
  16. George, W., 1979. Conservatism in the karyotypes of two African mole rats (Rodentia, Bathyergidae). Z. Sáugetierk. 44, 278–285.Google Scholar
  17. Gomes Rodrigues, H., Marangoni, P., Sumbera, R., Tafforeau, P., Wendelen, W., Viriot, L., 2011. Continuous dental replacement in a hyper-chisel tooth digging rodent. PNAS 108, 17355–17359.CrossRefGoogle Scholar
  18. Groves, C., Grubb, P., 2011. Ungulate Taxonomy. Johns Hopkins University Press, Baltimore, Maryland.Google Scholar
  19. Happold, D.C.D., 2013. Mammals of Africa - Volume III: Rodents, Hares and Rabbits. Bloomsbury Publishing, London.Google Scholar
  20. Heath, T.A., Huelsenbeck, J.P., Stadler, T., 2014. The fossilized birth-death process for coherent calibration of divergence-time estimates. PNAS 111, 2957–2966.CrossRefGoogle Scholar
  21. Huchon, D., Douzery, E.J., 2001. From the Old World to the New World: a molecular chronicle of the phylogeny and biogeography of hystricognath rodents. Mol. Phylogenet. Evol. 20, 238–251.CrossRefPubMedPubMedCentralGoogle Scholar
  22. Ingram, C.M., Burda, H., Honeycutt, R.L., 2004. Molecular phylogenetics and taxonomy of the African mole-rats, genus Cryptomys and the new genus Coetomys Gray, 1864. Mol. Phylogenet. Evol. 31, 997–1014.CrossRefPubMedPubMedCentralGoogle Scholar
  23. Jones, G., 2017. Algorithmic improvements to species delimitation and phylogeny estimation under the multispecies coalescent. J. Math. Biol. 74, 447–467.CrossRefPubMedPubMedCentralGoogle Scholar
  24. Jones, G., Aydin, Z., Oxelman, B., 2015. DISSECT: an assignment-free Bayesian discovery method for species delimitation under the multispecies coalescent. Bioinformatics 31, 991–998.CrossRefPubMedPubMedCentralGoogle Scholar
  25. Kopelman, N.M., Mayzel, J., Jakobsson, M., Rosenberg, N.A., Mayrose, I., 2015. CLUMPAK: a program for identifying clustering modes and packaging population structure inferences across. It Mol. Ecol. Res. 15, 1179–1191.CrossRefGoogle Scholar
  26. Larsson, A., 2014. AliView: a fast and lightweight alignment viewer and editor for large data sets. Bioinformatics 30, 3276–3278.CrossRefPubMedPubMedCentralGoogle Scholar
  27. Lavocat, R., 1973. Les rongeurs du Miocène d’Afrique Orientale. 1. Miocène Inférieure. Mém. Trav. E. P. H. E., Inst. Montpellier 1, pp. 1–284.Google Scholar
  28. Lawson, L.P., 2010. The discordance of diversification: evolution in the tropical-montane frogs of the Eastern Arc Mountains of Tanzania. Mol. Ecol. 19, 4046–4060.CrossRefPubMedPubMedCentralGoogle Scholar
  29. Linder, H.P., de Klerk, H.M., Born, J., Burgess, N.D., Fjeldsá, J., Rahbek, C., 2012. The partitioning of Africa: statistically defined biogeographical regions in sub-Saharan Africa. J. Biogeogr. 39, 1189–1205.CrossRefGoogle Scholar
  30. Lorenzen, E.D., Heller, R., Siegismund, H.R., 2012. Comparative phylogeography of African savannah ungulates. Mol. Ecol. 21, 3656–3670.CrossRefGoogle Scholar
  31. Mazoch, V., Mikula, O., Bryja, J., Konvicková, H., Russo, I.R., Verheyen, E., Sumbera, R., 2018. Phylogeography of a widespread sub-Saharan murid rodent Aethomys chrysophilus: the role of geographic barriers and paleoclimate in Zambezian region. Mammalia 82, 373–387.CrossRefGoogle Scholar
  32. McDonough, M.M., Sumbera, R., Mazoch, V., Ferguson, A.W., Phillips, C.D., Bryja, J., 2015. Multilocus phylogeography of a widespread savanna-woodland-adapted rodent reveals the influence of Pleistocene geomorphology and climate change in Africa’s Zambezi region. Mol. Ecol. 24, 5248–5266.CrossRefGoogle Scholar
  33. Mein, P., Pickford, M., 2003. Rodentia (other than Pedetidae) from the Orange River deposits, Namibia. Mem. Geol. Surv. Namibia 19, 147–160.Google Scholar
  34. Mikula, O., Sumbera, R., Aghová, T., Mbau, J.S., Katakweba, A.S., Sabuni, C.A., Bryja, J., 2016. Evolutionary history and species diversity of African pouched mice (Rodentia: Nesomyidae: Saccostomus). Zool. Scr. 45, 595–617.CrossRefGoogle Scholar
  35. Miller, M.A., Pfeiffer, W., Schwartz, T., 2010. Creating the CIPRES science gateway for inference of large phylogenetic trees. Proceedings of the Gateway Computing Environments Workshop (GCE), 1–8.Google Scholar
  36. Monadjem, A., Taylor, P.J., Denys, C., Cotterill, F.P.D., 2015. Rodents of Sub-Saharan Africa. A Biogeographic and Taxonomic Synthesis. Walter de Gruyter GmbH, Berlin/Munich/Boston.Google Scholar
  37. Musser, G.G., Carleton, M.D., 2005. Superfamily Muroidea. In: Wilson, D.E., Reeder, D.M. (Eds.), Mammal Species of the World., third edition. The Johns Hopkins University Press, pp. 894–1531.Google Scholar
  38. Ngalameno, M.K., Bastos, A.D.S., Mgode, G.F., Bennett, N.C., 2017. The pattern of reproduction Heliophobius from Tanzania: do not refrain during the long rains! Can. J. Zool. 95, 107–114.CrossRefGoogle Scholar
  39. Patzenhauerová, H., Bryja, J., Sumbera, R., 2010. Kinship structure and mating system in a solitary subterranean rodent, the silvery mole-rat. Behav. Ecol. Sociobiol. 64, 757–767.CrossRefGoogle Scholar
  40. Petruzela, J., Sumbera, R., Aghová, T., Bryjová, A., Katakweba, A.S., Sabuni, C.A., Chitaukali, W.N., Bryja, J., 2018. Spiny mice of the Zambezian bioregion - phylogeny, biogeography and ecological differentiation within the Acomys spinosissimus complex. Mammal. Biol. 91, 79–90.CrossRefGoogle Scholar
  41. Potts, R., 2013. Hominin evolution in settings of strong environmental variability. Quat. Sci. Rev. 73, 1–13.CrossRefGoogle Scholar
  42. Pritchard, J.K., Stephens, M., Donnelly, P., 2000. Inference of population structure using multilocus genotype data. Genetics 155, 945–959.PubMedPubMedCentralGoogle Scholar
  43. Puechmaille, S.J., 2016. The program structure does not reliably recoverthe correct population structure when sampling is uneven: subsampling and new estimators alleviate the problem. Mol. Ecol. Res. 16, 608–627.CrossRefGoogle Scholar
  44. Rambaut, A.J., Suchard, M.A., Xie, D., Drummond, A.J., Available from 2014. Tracer vl.6.
  45. Ronquist, F., Huelsenbeck, J.P., 2003. MrBayes3: Bayesian phylogenetic inference under mixed models. Bioinformatics 9, 1572–1574.CrossRefGoogle Scholar
  46. Rosenberg, N.A., 2004. Distruct: a program forthe graphical display of population structure. Mol. Ecol. Notes 4, 137–138.CrossRefGoogle Scholar
  47. Sabuni, C., Aghová, T., Bryjová, A., Sumbera, R., Bryja, J., 2018. Biogeographic implications of small mammals from Northern Highlands in Tanzania with first data from the volcanic Mount Kitumbeine. Mammalia 82, 360–372.CrossRefGoogle Scholar
  48. Scharff, A., Macholán, M., Burda, H., 2001. A new karyotype of Heliophobius argenteocinereus (Bathyergidae, Rodentia) from Zambia with field notes on the species. Z. Saugetierkd. 66, 376–378.Google Scholar
  49. Schenk, J.J., 2016. Consequences of secondary calibrations on divergence time estimates. PLoS One 11, e0148228.CrossRefPubMedPubMedCentralGoogle Scholar
  50. Stamatakis, A., 2014. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phytogenies. Bioinformatics 30, 1312–1313.CrossRefPubMedPubMedCentralGoogle Scholar
  51. Sumbera, R., Burda, H., Chitaukali, W.N., 2007. Biology of the silvery mole-rat (Heliophobius argenteocinereus). Why study a neglected subterranean rodent species? In: Begall, S., Burda, H., Schleich, C.E. (Eds.), Subterranean Rodents: News from Underground. Springer, London, pp. 221–236.CrossRefGoogle Scholar
  52. Swynnerton, G.H., 1945. A revision of the type-localities of mammals occurring in the Tanganyika territory. J. Zool. 115, 49–84.Google Scholar
  53. Tamura, K., Stecher, G., Peterson, D., Filipski, A., Kumar, S., 2013. MEGA6: molecular evolutionary genetics analysis version 6.0. Mol. Biol. Evol. 30, 2725–2729.CrossRefPubMedPubMedCentralGoogle Scholar
  54. Trauth, M.H., Larrasoana, J.C., Mudelsee, M., 2009. Trends, rhythms and events in Plio-Pleistocene African climate. Quat. Sci. Rev. 28, 399–411.CrossRefGoogle Scholar
  55. Van Daele, P.A.A.G., Verheyen, E., Brunain, M., Adriaens, D., 2007. ytochrome b sequence analysis reveals differential molecular evolution in African mole-rats of the chromosomally hyperdiverse genus Fukomys (Bathyergidae, Rodentia) from the Zambezian region. Mol. Phylogenet. Evol. 45, 142–157.CrossRefPubMedPubMedCentralGoogle Scholar
  56. Verheyen, W., Hulselmans, J., Dierckx, T., Mulungu, L., Leirs, H., Corti, M., Verheyen, E., 2007. The characterization of the Kilimanjaro Lophuromys aquiius True 1892 population and the description of five new Lophuromys species (Rodentia, Muridae). Bulletin van het Koninklijk Belgisch Instituut voor Natuurwetenschappen, Biologie 77, 23–75.Google Scholar
  57. Verheyen, W., Hulselmans, J., Wendelen, W., Leirs, H., Corti, M., Backeljau, T., Verheyen, E., 2011. Contribution to the systematics and zoogeography of the East-African Acomys spinosissimus Peters 1852 species complex and the description of two new species (Rodentia: Muridae). Zootaxa 3059, 1–35.CrossRefGoogle Scholar
  58. Winkler, A.J., Denys, C., Avery, D.M., 2010. Chapter 17: Rodentia. In: Werdelin, L., Sanders, W.J. (Eds.), Cenozoic Mammals of Africa. University of California Press, Berkeley, pp. 263–304.Google Scholar
  59. Zachos, F.E., 2016. Species Concepts in Biology. In: Historical Development, Theoretical Foundations and Practical Relevance. Springer International Publishing, Switzerland.Google Scholar
  60. Zachos, F.E., Apollonio, M., Bármann, E.V., Festa-Bianchet, M., Góhlich, U., Habel, J.C., Haring, E., Kruckenhauser, L., Lovari, S., McDevitt, Allan D., Pertoldi, C., Róssner, G.E., Sánchez-Villagra, M.R., Scandura, M., Suchentrunk, F., 2013. Species inflation and taxonomic artefacts—a critical comment on recent trends in mammalian classification. Mammal. Biol. 78, 1–6.CrossRefGoogle Scholar

Copyright information

© Deutsche Gesellschaft für Säugetierkunde 2018

Authors and Affiliations

  • Josef Bryja
    • 1
    • 2
    • 7
    Email author
  • Hana Konvičková
    • 1
  • Anna Bryjová
    • 1
  • Ondřej Mikula
    • 1
    • 3
  • Rhodes Makundi
    • 4
  • Wilbert N. Chitaukali
    • 5
  • Radim šumbera
    • 6
  1. 1.Institute of Vertebrate Biology of the Czech Academy of SciencesBrnoCzech Republic
  2. 2.Department of Botany and Zoology, Faculty of ScienceMasaryk UniversityBrnoCzech Republic
  3. 3.Institute of Animal Physiology and Genetics of the Czech Academy of ScienceBrnoCzech Republic
  4. 4.Pest Management CenterSokoine University of AgricultureMorogoroTanzania
  5. 5.Biology Department, Chancellor CollegeUniversity of MalawiZombaMalawi
  6. 6.Department of Zoology, Faculty of ScienceUniversity of South BohemiaCeské BudëjoviceCzech Republic
  7. 7.Institute of Vertebrate Biology of the Academy of Sciences of the Czech Republic.Research Facility StudeneC.KonësínCzech Republic

Personalised recommendations